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Question: What does Jesus mean when he said in Matthew 10:16b: "be ye therefore wise as serpents, and harmless as doves."

“Behold, I send you forth as sheep in the midst of wolves: be ye therefore wise as serpents, and harmless as doves.” (Matthew 10:16, AV)

Answer: The above similes (being wise as serpents and harmless as doves) describe the Christian’s prescribed behavior in — what was certainly then and continues to be now — a world that is hostile to believers… but not incidentally hostile… it is purposefully hostile as in, “sheep among wolves” (Matthew 10:16a). The question becomes then, how can we advance the kingdom of God effectively without becoming predatory ourselves?... and that’s what I believe Jesus was teaching: To be Christ-like in a godless world requires that we combine (what was understood to be) the wisdom of the serpent with the harmlessness of the dove.

Nineteenth-century divine, Charles Simeon, gave us the perfect overview of this section:

“The serpent is said to be “more subtle than all the beasts of the field:” and the dove is proverbially kind and innocent. Now the wisdom of the one and the harmlessness of the other are very desirable to be combined in the Christian character; because it is by such an union only that the Christian will be enabled to cope successfully with his more powerful enemies.”

Now, I am not sure what drove your question — whether or not you were surprised by Jesus’ evoking the image of a serpent… which carries some baggage from the Garden of Eden (Genesis 3:1). But we should not make too much of that connection here. The same characteristics existed in the serpent then and now, but we cannot attach the evil actions of Satan (as the serpent) with the serpent itself. Creatures that are non-human and non-angelic are not moral entities. So, the creature itself cannot perform sin… but the image of Satan’s shrewdness did indeed stick to this maligned creature — and shrewdness (without the sin) is an asset, not a defect… and that was what Jesus was invoked in this teaching.

As to the literature, the serpent simile stands in Jesus’ dialogue without bringing forward any of the serpent’s pejoratives. By what rule? It is a properly basic understanding in language that when a speaker creates a simile, he is not (necessarily) invoking the entire potential of the words he has chosen — nor is he invoking the entire history of its vehicle and tenor. He is defining a fresh relationship. So, a quick look at our passage tells us that Jesus was invoking only the positive aspects of the serpent. There is no hint that he was unloading Edenic baggage upon his disciples. So, what was Jesus doing here?

He was making a general statement about the technique of kingdom work. These are the overarching principles that should guide us as we bring the gospel to a hostile world. Jesus was not suggesting that we stoop to behaviors like deception (as was exemplified in Satan’s manifestation as a serpent), but rather that we should model some of its shrewdness in a positive way. Let us consider Jesus as exemplar.

Jesus was known to be a gentle person. Indeed, Scripture testifies that he would not even quench a smoking flax (Matthew 12:20). But was he always (and only) gentle? No.

“Jesus entered the temple courts and drove out all who were buying and selling there. He overturned the tables of the money changers and the benches of those selling doves. “It is written,” he said to them, “ ‘My house will be called a house of prayer,’ but you are making it ‘a den of robbers.’” (Matthew 21:12–13, NIV)

Now, people were always doing this kind of stuff at the temple. So why did Jesus choose a physical confrontation for that particular moment? Because, although he was harmless as a dove, he was also as wise as a serpent… and this cleansing simply had to be done — so he did it! But this is the kind of “statement” you only have to make once… and this was the teachable moment. But when you consider this extraordinarily rare action in light of his usual mien, you begin to see the power in using a combination of tools: since Jesus rarely did this, this “dove of a man” spoke more loudly than any thug.

In his more typical moments, Jesus also showed that he was wise as a serpent by the way he taught. He knew enough to discern the differences in his audiences (a critical skill), and he used the technique of “speaking in parables” to both feed and weed.

“When he was alone, the Twelve and the others around him asked him about the parables. He told them, “The secret of the kingdom of God has been given to you. But to those on the outside everything is said in parables so that, “ ‘they may be ever seeing but never perceiving, and ever hearing but never understanding; otherwise they might turn and be forgiven!’”” (Mark 4:10–12, NIV)

A postmodern reader might think it is somehow “unfair” of Jesus to limit his audience this way. But, he knew that those who did not “have an ear” would either not process his words correctly… or process them towards evil! A harmless dove cannot discern when a “pearls before swine” should apply (Matthew 7:6). The serpent can.

Now let us examine the saddest example of all — the events before Jesus’ crucifixion. In this passage, he both speaks the truth to a hostile audience and remains harmless as a dove at the same time… and we know the result.

“Then the high priest stood up and said to Jesus, “Are you not going to answer? What is this testimony that these men are bringing against you?” …. Tell us if you are the Messiah, the Son of God.” “You have said so,” Jesus replied. “But I say to all of you: From now on you will see the Son of Man sitting at the right hand of the Mighty One and coming on the clouds of heaven.” Then the high priest tore his clothes and said, “He has spoken blasphemy!....” (Matthew 26:62–65, NIV)

Jesus paid the price for his “setting aside” of any serpent-like shrewdness at that moment. He spoke hard truth to the religious establishment… to those who did not “have an ear.” They called the truth blasphemy; they killed the Lord of glory… and they will kill us, too… if we are not as wise as serpents.

Now, we may be called to lay down our lives like this someday — and many already have. But in Matthew 10:16, Jesus did not have death in view. He was teaching us how to optimize our kingdom-spreading opportunities. He was encouraging us to count the cost of passivity vs. action — between direct speech and circumspection.

As a final thought, people see the dove as gentle— and why not. It is easy to see, easy to hold… and easy to sacrifice (Leviticus 14:30). It is a “clean” bird under the Levitical law. But people see the serpent as sneaky and opportunistic. So, with stealth as its primary weapon, the serpent is not easy to see… and it’s creepy to hold! Furthermore, it was “unclean” and not acceptable for Levitical sacrifice (Leviticus 11:42). But now I must ask, by invoking the serpent, was Jesus telling us to “fight dirty?”

No. He was telling us to “fight smart.”… to know when to fight… when to shake off the dust (Matthew 10:14), when to stand, when to sacrifice…

Successful Christian living requires that we find the optimal balance between the dove and the serpent. We should strive to be gentle and sacrificial… but without being doormats. And we should strive to tell the world about Jesus… but without being jerks. In my opinion, that was Jesus’ emphasis when he used the serpent and dove comparison.